{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T22:44:56Z","timestamp":1759963496054,"version":"3.37.3"},"reference-count":29,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,1,30]],"date-time":"2019-01-30T00:00:00Z","timestamp":1548806400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,1,30]],"date-time":"2019-01-30T00:00:00Z","timestamp":1548806400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>This paper is part of the emerging field of Evolutionary Developmental Pathology, dedicated to study the links between normal and abnormal development, evolution and human pathologies. We analyzed the head musculoskeletal system of several \u2018natural mutant\u2019 newborn lambs displaying various degrees of abnormality, from mild defects to <jats:italic>cebocephaly<\/jats:italic> and to <jats:italic>cyclopia<\/jats:italic>, and compared them with humans. Interestingly, muscle defects are less marked than osteological ones, and contrarily to the latter they tend to display left-right assymetries. In individuals with cebocephalic and even cyclopic skulls almost all head muscles are normal. The very few exceptions are some extraocular muscles and facial muscles that normally attach to osteological structures that are missing in the abnormal heads: such muscles are instead attached to the \u2018nearest topological neighbor\u2019 of the missing osteological structure, a pattern also found in cyclopic humans. These observations support Alberch\u2019s ill-named \u201clogic of monsters\u201d - as a byproduct of strong developmental\/topological constraints anatomical patterns tend to repeat themselves, even severe malformations displayed by distantly related taxa. They also support the idea that mammalian facial muscles reverted to an ancestral \u2018nearest-neighbor\u2019 muscle-bone type of attachment seen in non-vertebrate animals and in vertebrate limbs, but not in other vertebrate head muscles.<\/jats:p>","DOI":"10.1038\/s41598-018-37735-9","type":"journal-article","created":{"date-parts":[[2019,1,30]],"date-time":"2019-01-30T11:04:42Z","timestamp":1548846282000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Musculoskeletal study of cebocephalic and cyclopic lamb heads illuminates links between normal and abnormal development, evolution and human pathologies"],"prefix":"10.1038","volume":"9","author":[{"given":"Rui","family":"Diogo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1194-4766","authenticated-orcid":false,"given":"Daria","family":"Razmadze","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalia","family":"Siomava","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nora","family":"Douglas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jose S. M.","family":"Fuentes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andre","family":"Duerinckx","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2019,1,30]]},"reference":[{"key":"37735_CR1","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1007\/s11692-014-9296-1","volume":"42","author":"G Guinard","year":"2015","unstructured":"Guinard, G. Introduction to evolutionary teratology, with an application to the forelimbs of tyrannosauridae and carnotaurinae (Dinosauria: Theropoda). Evol. Biol. 42, 20\u201341 (2015).","journal-title":"Evol. Biol."},{"key":"37735_CR2","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1111\/joa.12301","volume":"226","author":"R Diogo","year":"2015","unstructured":"Diogo, R., Walsh, S., Smith, C., Ziermann, J. M. & Abdala, V. Towards the resolution of a long-standing evolutionary question: muscle identity and attachments are mainly related to topological position and not to primordium or homeotic identity of digits. J. Anat. 226, 523\u2013529 (2015a).","journal-title":"J. Anat."},{"key":"37735_CR3","doi-asserted-by":"publisher","first-page":"1357","DOI":"10.1002\/dvdy.24336","volume":"244","author":"R Diogo","year":"2015","unstructured":"Diogo, R., Smith, C. & Ziermann, J. M. Evolutionary Developmental Pathology and Anthropology: a new area linking development, comparative anatomy, human evolution, morphological variations and defects, and medicine. Dev. Dyn. 244, 1357\u20131374 (2015b).","journal-title":"Dev. Dyn."},{"key":"37735_CR4","unstructured":"Smith, C. M. et al. Muscular and skeletal anomalies in human trisomy in an evo-devo context: description of a T18 cyclopic newborn and comparison between Edwards (T18), Patau (T13) and Down (T21) syndromes using 3-D imaging and anatomical illustrations. (Taylor & Francis, 2015)."},{"key":"37735_CR5","first-page":"706","volume":"13","author":"HE Evans","year":"1966","unstructured":"Evans, H. E., Ingalls, T. H. & Binns, W. Teratogenesis of craniofacial malformations in animals. III. Natural and experimental cephalic deformities in sheep. Arch. Environ. Health 13, 706\u2013714 (1966).","journal-title":"Natural and experimental cephalic deformities in sheep. Arch. Environ. Health"},{"key":"37735_CR6","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1002\/tera.1420420404","volume":"42","author":"JP Souza","year":"1990","unstructured":"Souza, J. P., Siebert, J. R. & Beckwith, J. B. An anatomic comparison of cebocephaly and ethmocephaly. Teratology 42, 347\u2013357 (1990).","journal-title":"Teratology"},{"key":"37735_CR7","first-page":"229","volume":"178","author":"P Kruszka","year":"2018","unstructured":"Kruszka, P. & Muenke, M. Syndromes associated with holoprosencephaly. AJMG 178, 229\u2013237 (2018).","journal-title":"AJMG"},{"key":"37735_CR8","first-page":"180","volume":"134","author":"W Binns","year":"1959","unstructured":"Binns, W., James, L. F., Shupe, J. L. & Everett, G. A Congenital Cyclopian-Type Malformation in Lambs. J. Amer. Vet. Med. Assoc. 134, 180\u2013183 (1959).","journal-title":"J. Amer. Vet. Med. Assoc."},{"key":"37735_CR9","first-page":"515","volume":"137","author":"W Binns","year":"1960","unstructured":"Binns, W., Anderson, W. A. & Sullivan, D. J. Further Observations on a Congenital Cyclopian-Type Malformation in Lambs. J. Amer. Vet. Med. Assoc. 137, 515\u2013521 (1960).","journal-title":"J. Amer. Vet. Med. Assoc."},{"key":"37735_CR10","first-page":"1164","volume":"24","author":"W Binns","year":"1963","unstructured":"Binns, W., James, L. F., Shupe, J. L. & Everett, G. A Congenital Cyclopian-Type Malformation in Lambs Induced by Maternal Ingestion of a Range Plant. Veratrum califomicum. Amer. J. Vet. Res. 24, 1164\u20131175 (1963).","journal-title":"Veratrum califomicum. Amer. J. Vet. Res."},{"key":"37735_CR11","first-page":"839","volume":"147","author":"W Binns","year":"1965","unstructured":"Binns, W., James, L. F., Shupe, J. L. & Everett, G. Chronological Evaluation of Teratogenicity in Sheep Fed with Veratrum califomicum. J. Amer. Vet. Med. Assoc. 147, 839\u2013842 (1965).","journal-title":"J. Amer. Vet. Med. Assoc."},{"key":"37735_CR12","doi-asserted-by":"crossref","unstructured":"James, L. F., Panter, K. E., Gaffield, W., Molyneux, R. J. & Weinzweig, J. Poisonous plant research: Biomedical applications. In Poisonous Plants and Related Toxins, pp. 361\u2013376 (eds Acamovic, T., Stewart, C. S. & Pennycott, T. W.), (CABI International, 2004).","DOI":"10.1079\/9780851996141.0361"},{"key":"37735_CR13","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/S0016-6995(89)80006-3","volume":"12","author":"P Alberch","year":"1989","unstructured":"Alberch, P. The logic of monsters: evidence for internal constraint in development and evolution. Geobios M\u00e9m. Sp\u00e9c. 12, 21\u201357 (1989).","journal-title":"Geobios M\u00e9m. Sp\u00e9c."},{"key":"37735_CR14","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1002\/jez.b.22709","volume":"328","author":"R Diogo","year":"2017","unstructured":"Diogo, R., Guinard, G. & Diaz, R. Dinosaurs, chameleons, humans and Evo-Devo-Path: linking \u00c9tienne Geoffroy\u2019s teratology, Waddington\u2019s homeorhesis, Alberch\u2019s logic of \u2018monsters\u2019, and Goldschmidt hopeful \u2018monsters\u2019. J. Exp. Zool. B 328, 207\u2013229 (2017).","journal-title":"J. Exp. Zool. B"},{"key":"37735_CR15","doi-asserted-by":"crossref","first-page":"3229","DOI":"10.1242\/dev.122.10.3229","volume":"122","author":"G K\u00f6ntges","year":"1996","unstructured":"K\u00f6ntges, G. & Lumsden, A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122, 3229\u20133242 (1996).","journal-title":"Development"},{"key":"37735_CR16","doi-asserted-by":"crossref","unstructured":"Diogo, R. & Abdala, V. Muscles of vertebrates: comparative anatomy, evolution, homologies and development (Taylor & Francis, 2010).","DOI":"10.1201\/9781439845622"},{"key":"37735_CR17","unstructured":"Diogo, R., Ziermann, J. M., Molnar, J., Siomava, N. & Abdala, V. Chordate muscles: development, homologies and evolution (Taylor & Francis, 2018)."},{"key":"37735_CR18","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1111\/j.1469-7580.2011.01403.x","volume":"219","author":"R Diogo","year":"2011","unstructured":"Diogo, R. & Wood, B. Soft-tissue anatomy of the primates: phylogenetic analyses based on the muscles of the head, neck, pectoral region and upper limb, with notes on the evolution of these muscles. J. Anat. 219, 273\u2013359 (2011).","journal-title":"J. Anat."},{"key":"37735_CR19","doi-asserted-by":"crossref","unstructured":"Diogo, R & Wood, B. Comparative anatomy and phylogeny of primate muscles and human evolution, (Taylor and Francis, 2012a).","DOI":"10.1201\/b11605"},{"key":"37735_CR20","doi-asserted-by":"publisher","first-page":"3267","DOI":"10.1111\/j.1558-5646.2012.01621.x","volume":"66","author":"R Diogo","year":"2012","unstructured":"Diogo, R. & Wood, B. Violation of Dollo\u2019s Law: Evidence of muscle reversions in primate phylogeny and their implications for the understanding of the ontogeny, evolution and anatomical variations of modern humans. Evolution 66, 3267\u20133276 (2012b).","journal-title":"Evolution"},{"key":"37735_CR21","doi-asserted-by":"publisher","first-page":"988","DOI":"10.1111\/brv.12039","volume":"88","author":"R Diogo","year":"2013","unstructured":"Diogo, R. & Wood, B. The broader evolutionary lessons to be learned from a comparative and phylogenetic analysis of primate muscle morphology. Biol. Rev. 88, 988\u20131001 (2013).","journal-title":"Biol. Rev."},{"key":"37735_CR22","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1163\/1570756042729492","volume":"54","author":"R Diogo","year":"2004","unstructured":"Diogo, R. Muscles versus bones: catfishes as a case study for an analysis on the contribution of myological and osteological structures in phylogenetic reconstructions. Anim. Biol. 54, 373\u2013391 (2004).","journal-title":"Anim. Biol."},{"key":"37735_CR23","doi-asserted-by":"publisher","first-page":"582","DOI":"10.1002\/dvdy.20177","volume":"231","author":"C Prunotto","year":"2004","unstructured":"Prunotto, C. et al. Analysis of Mlc-lacZ Met mutants highlights the essential function of Met for migratory precursors of hypaxial muscles and reveals a role for Met in the development of hyoid arch-derived facial muscles. Dev. Dyn. 231, 582\u2013591 (2004).","journal-title":"Dev. Dyn."},{"key":"37735_CR24","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1002\/ar.1090280303","volume":"28","author":"RR Humphrey","year":"1924","unstructured":"Humphrey, R. R. A case of cyclopia in homo. Anat. Rec. 28, 207\u2013225 (1924).","journal-title":"Anat. Rec."},{"key":"37735_CR25","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1002\/tera.1420260202","volume":"26","author":"VG Kokich","year":"1982","unstructured":"Kokich, V. G., Ngim, C.-H., Siebert, J. R., Clarren, S. K. & Cohen, M. M. Cyclopia: An anatomic and histologic study of two specimens. Teratology 26, 105\u2013113 (1982).","journal-title":"Teratology"},{"key":"37735_CR26","first-page":"135","volume":"9","author":"KR Fisher","year":"1989","unstructured":"Fisher, K. R., Partlow, G. D. & Holmes, C. J. Anatomical observations of holoprosencephaly in swine. J. Craniofac. Genet. Dev. Biol. 9, 135\u2013146 (1989).","journal-title":"J. Craniofac. Genet. Dev. Biol."},{"key":"37735_CR27","doi-asserted-by":"publisher","first-page":"2157","DOI":"10.1002\/ar.22589","volume":"295","author":"R Diogo","year":"2012","unstructured":"Diogo, R. et al. The head and neck muscles of the serval and tiger: homologies, evolution and proposal of a mammalian and a veterinary muscle ontology. Anat. Rec. 295, 2157\u20132178 (2012).","journal-title":"Anat. Rec."},{"key":"37735_CR28","unstructured":"Getty, R. Sisson and Grossman\u2019s The anatomy of the domestic animals, 5th edition, (Saunders, 1975)."},{"key":"37735_CR29","unstructured":"May, N. D. S. The anatomy of the sheep, 2nd edition (University of Queensland Press, 1964)."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37735-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37735-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37735-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T05:13:33Z","timestamp":1671254013000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-37735-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,1,30]]},"references-count":29,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["37735"],"URL":"https:\/\/doi.org\/10.1038\/s41598-018-37735-9","relation":{},"ISSN":["2045-2322"],"issn-type":[{"type":"electronic","value":"2045-2322"}],"subject":[],"published":{"date-parts":[[2019,1,30]]},"assertion":[{"value":"16 March 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 December 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 January 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"991"}}